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Published in: Documenta Ophthalmologica 1/2010

01-02-2010 | REVIEW ARTICLE

Understanding ischemic retinopathies: emerging concepts from oxygen-induced retinopathy

Authors: Elsa Kermorvant-Duchemin, Przemyslaw Sapieha, Mirna Sirinyan, Martin Beauchamp, Daniella Checchin, Pierre Hardy, Florian Sennlaub, Pierre Lachapelle, Sylvain Chemtob

Published in: Documenta Ophthalmologica | Issue 1/2010

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Abstract

Ischemic retinopathies, such as retinopathy of prematurity and diabetic retinopathy are characterized by an initial microvascular degeneration, followed by an abnormal hypoxia-induced neovascularization. Oxygen-induced retinopathy (OIR) is a well-established in vivo model of ischemic retinopathies, which, although the triggering insult varies, all share a common end result of capillary loss. Understanding the mechanisms of normal retinal vascular development as well as the pathophysiological processes leading to the primary vascular loss is the key to develop treatments to prevent the sight-threatening neovascularization associated with human ischemic retinopathies. The importance of oxygen-dependant vascular endothelial growth factor in the pathophysiology of both phases of OIR has long been recognized. However, recent studies point out that OIR is a multifactorial disease, resulting from additive effects of an unbalanced expression of pro- and anti-angiogenic factors, interrelated with protective effects of nutritional factors and cytotoxic effects of oxidative and nitro-oxidative stress-dependant mediators. This review summarizes the most recent aspects of the research on OIR conducted in our laboratory and others, with a particular focus on the role of new mediators of nitro-oxidative stress, the trans-arachidonic acids, in microvascular degeneration, and on a novel pathway of metabolic signaling where hypoxia-driven succinate, via receptor GPR91, governs normal and pathological retinal angiogenesis.
Literature
1.
go back to reference Penn JS, Tolman BL, Lowery LA (1993) Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci 34:576–585PubMed Penn JS, Tolman BL, Lowery LA (1993) Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci 34:576–585PubMed
2.
go back to reference Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35:3429–3435PubMed Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35:3429–3435PubMed
3.
go back to reference Smith LE, Wesolowski E, McLellan A, Kostyk SK, D’Amato R, Sullivan R, D’Amore PA (1994) Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35:101–111PubMed Smith LE, Wesolowski E, McLellan A, Kostyk SK, D’Amato R, Sullivan R, D’Amore PA (1994) Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35:101–111PubMed
4.
go back to reference Chan-Ling T, Tout S, Hollander H, Stone J (1992) Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 33:2128–2147PubMed Chan-Ling T, Tout S, Hollander H, Stone J (1992) Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 33:2128–2147PubMed
5.
go back to reference McLeod DS, D’Anna SA, Lutty GA (1998) Clinical and histopathologic features of canine oxygen-induced proliferative retinopathy. Invest Ophthalmol Vis Sci 39:1918–1932PubMed McLeod DS, D’Anna SA, Lutty GA (1998) Clinical and histopathologic features of canine oxygen-induced proliferative retinopathy. Invest Ophthalmol Vis Sci 39:1918–1932PubMed
6.
go back to reference Gyllensten LJ, Hellstrom BE (1954) Experimental approach to the pathogenesis of retrolental fibroplasia. I. Changes of the eye induced by exposure of newborn mice to concentrated oxygen. Acta Paediatr 43:131–148CrossRef Gyllensten LJ, Hellstrom BE (1954) Experimental approach to the pathogenesis of retrolental fibroplasia. I. Changes of the eye induced by exposure of newborn mice to concentrated oxygen. Acta Paediatr 43:131–148CrossRef
7.
go back to reference Alon T, Hemo I, Itin A, Pe’er J, Stone J, Keshet E (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024–1028CrossRefPubMed Alon T, Hemo I, Itin A, Pe’er J, Stone J, Keshet E (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024–1028CrossRefPubMed
8.
go back to reference Pierce EA, Foley ED, Smith LE (1996) Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity [erratum 1997, 115:427]. Arch Ophthalmol 114:1219–1228PubMed Pierce EA, Foley ED, Smith LE (1996) Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity [erratum 1997, 115:427]. Arch Ophthalmol 114:1219–1228PubMed
9.
go back to reference Stone J, Chan-Ling T, Pe’er J, Itin A, Gnessin H, Keshet E (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37:290–299PubMed Stone J, Chan-Ling T, Pe’er J, Itin A, Gnessin H, Keshet E (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37:290–299PubMed
10.
go back to reference Simons BD, Flynn JT (1999) Retinopathy of prematurity and associated factors. Int Ophthalmol Clin 39:29–48CrossRefPubMed Simons BD, Flynn JT (1999) Retinopathy of prematurity and associated factors. Int Ophthalmol Clin 39:29–48CrossRefPubMed
11.
go back to reference Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-1) and type 1 IGF receptor (IGF-1R). Cell 75:59–72PubMed Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (IGF-1) and type 1 IGF receptor (IGF-1R). Cell 75:59–72PubMed
12.
go back to reference Lassarre C, Hardouin S, Daffos F, Forestier F, Frankenne F, Binoux M (1991) Serum insulin-like growth factors and insulin-like growth factor binding proteins in the human fetus. Relationships with growth in normal subjects and in subjects with intrauterine growth retardation. Pediatr Res 29:219–225CrossRefPubMed Lassarre C, Hardouin S, Daffos F, Forestier F, Frankenne F, Binoux M (1991) Serum insulin-like growth factors and insulin-like growth factor binding proteins in the human fetus. Relationships with growth in normal subjects and in subjects with intrauterine growth retardation. Pediatr Res 29:219–225CrossRefPubMed
13.
go back to reference Reece EA, Wiznitzer A, Le E, Homko CJ, Behrman H, Spencer EM (1994) The relation between human fetal growth and fetal blood levels of insulin-like growth factors I and II, their binding proteins, and receptors. Obstet Gynecol 84:88–95PubMed Reece EA, Wiznitzer A, Le E, Homko CJ, Behrman H, Spencer EM (1994) The relation between human fetal growth and fetal blood levels of insulin-like growth factors I and II, their binding proteins, and receptors. Obstet Gynecol 84:88–95PubMed
14.
go back to reference Langford K, Nicolaides K, Miell JP (1998) Maternal and fetal insulin-like growth factors and their binding proteins in the second and third trimesters of human pregnancy. Hum Reprod 13:1389–1393CrossRefPubMed Langford K, Nicolaides K, Miell JP (1998) Maternal and fetal insulin-like growth factors and their binding proteins in the second and third trimesters of human pregnancy. Hum Reprod 13:1389–1393CrossRefPubMed
15.
go back to reference Lineham JD, Smith RM, Dahlenburg GW, King RA, Haslam RR, Stuart MC, Faull L (1986) Circulating insulin-like growth factor I levels in newborn premature and full-term infants followed longitudinally. Early Hum Dev 13:37–46CrossRefPubMed Lineham JD, Smith RM, Dahlenburg GW, King RA, Haslam RR, Stuart MC, Faull L (1986) Circulating insulin-like growth factor I levels in newborn premature and full-term infants followed longitudinally. Early Hum Dev 13:37–46CrossRefPubMed
16.
go back to reference Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, LeRoith D, Senger DR, Smith LE (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci U S A 98:5804–5808CrossRefPubMed Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, LeRoith D, Senger DR, Smith LE (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci U S A 98:5804–5808CrossRefPubMed
17.
go back to reference Hellstrom A, Engstrom E, Hard AL, Albertsson-Wikland K, Carlsson B, Niklasson A, Lofqvist C, Svensson E, Holm S, Ewald U, Holmstrom G, Smith LE (2003) Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics 112:1016–1020CrossRefPubMed Hellstrom A, Engstrom E, Hard AL, Albertsson-Wikland K, Carlsson B, Niklasson A, Lofqvist C, Svensson E, Holm S, Ewald U, Holmstrom G, Smith LE (2003) Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics 112:1016–1020CrossRefPubMed
18.
go back to reference Lofqvist C, Andersson E, Sigurdsson J, Engstrom E, Hard AL, Niklasson A, Smith LE, Hellstrom A (2006) Longitudinal postnatal weight and insulin-like growth factor I measurements in the prediction of retinopathy of prematurity. Arch Ophthalmol 124:1711–1718CrossRefPubMed Lofqvist C, Andersson E, Sigurdsson J, Engstrom E, Hard AL, Niklasson A, Smith LE, Hellstrom A (2006) Longitudinal postnatal weight and insulin-like growth factor I measurements in the prediction of retinopathy of prematurity. Arch Ophthalmol 124:1711–1718CrossRefPubMed
19.
go back to reference Smith LE, Kopchick JJ, Chen W, Knapp J, Kinose F, Daley D, Foley E, Smith RG, Schaeffer JM (1997) Essential role of growth hormone in ischemia-induced retinal neovascularization. Science 276:1706–1709CrossRefPubMed Smith LE, Kopchick JJ, Chen W, Knapp J, Kinose F, Daley D, Foley E, Smith RG, Schaeffer JM (1997) Essential role of growth hormone in ischemia-induced retinal neovascularization. Science 276:1706–1709CrossRefPubMed
20.
go back to reference Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, Schaeffer JM, Senger DR (1999) Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 5:1390–1395CrossRefPubMed Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, Schaeffer JM, Senger DR (1999) Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 5:1390–1395CrossRefPubMed
21.
go back to reference Frystyk J (2004) Free insulin-like growth factors–measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 14:337–375CrossRefPubMed Frystyk J (2004) Free insulin-like growth factors–measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 14:337–375CrossRefPubMed
22.
go back to reference Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23:824–854CrossRefPubMed Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23:824–854CrossRefPubMed
23.
go back to reference Lofqvist C, Chen J, Connor KM, Smith AC, Aderman CM, Liu N, Pintar JE, Ludwig T, Hellstrom A, Smith LE (2007) IGFBP3 suppresses retinopathy through suppression of oxygen-induced vessel loss and promotion of vascular regrowth. Proc Natl Acad Sci U S A 104:10589–10594CrossRefPubMed Lofqvist C, Chen J, Connor KM, Smith AC, Aderman CM, Liu N, Pintar JE, Ludwig T, Hellstrom A, Smith LE (2007) IGFBP3 suppresses retinopathy through suppression of oxygen-induced vessel loss and promotion of vascular regrowth. Proc Natl Acad Sci U S A 104:10589–10594CrossRefPubMed
25.
go back to reference Jaquet K, Krause K, Tawakol-Khodai M, Geidel S, Kuck KH (2002) Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc Res 64:326–333CrossRefPubMed Jaquet K, Krause K, Tawakol-Khodai M, Geidel S, Kuck KH (2002) Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc Res 64:326–333CrossRefPubMed
26.
go back to reference Ribatti D, Presta M, Vacca A, Ria R, Giuliani R, Dell’Era P, Nico B, Roncali L, Dammacco F (1999) Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 93:2627–2636PubMed Ribatti D, Presta M, Vacca A, Ria R, Giuliani R, Dell’Era P, Nico B, Roncali L, Dammacco F (1999) Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 93:2627–2636PubMed
27.
go back to reference Brines M, Cerami A (2005) Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 6:484–494CrossRefPubMed Brines M, Cerami A (2005) Emerging biological roles for erythropoietin in the nervous system. Nat Rev Neurosci 6:484–494CrossRefPubMed
28.
go back to reference Chen J, Connor KM, Aderman CM, Smith LE (2008) Erythropoietin deficiency decreases vascular stability in mice. J Clin Invest 118:526–533PubMed Chen J, Connor KM, Aderman CM, Smith LE (2008) Erythropoietin deficiency decreases vascular stability in mice. J Clin Invest 118:526–533PubMed
29.
go back to reference Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE (2009) Erythropoietin siRNA suppresses retinal neovascularization in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci. doi:10.1167/iovs.1108-2521 Chen J, Connor KM, Aderman CM, Willett KL, Aspegren OP, Smith LE (2009) Erythropoietin siRNA suppresses retinal neovascularization in a mouse model of proliferative retinopathy. Invest Ophthalmol Vis Sci. doi:10.​1167/​iovs.​1108-2521
30.
go back to reference Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, Kobayashi T, Masuda S, Nagao M, Yoshimura N, Takagi H (2005) Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 353:782–792CrossRefPubMed Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, Kobayashi T, Masuda S, Nagao M, Yoshimura N, Takagi H (2005) Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 353:782–792CrossRefPubMed
31.
go back to reference Katsura Y, Okano T, Matsuno K, Osako M, Kure M, Watanabe T, Iwaki Y, Noritake M, Kosano H, Nishigori H, Matsuoka T (2005) Erythropoietin is highly elevated in vitreous fluid of patients with proliferative diabetic retinopathy. Diabetes Care 28:2252–2254CrossRefPubMed Katsura Y, Okano T, Matsuno K, Osako M, Kure M, Watanabe T, Iwaki Y, Noritake M, Kosano H, Nishigori H, Matsuoka T (2005) Erythropoietin is highly elevated in vitreous fluid of patients with proliferative diabetic retinopathy. Diabetes Care 28:2252–2254CrossRefPubMed
32.
go back to reference Suk KK, Dunbar JA, Liu A, Daher NS, Leng CK, Leng JK, Lim P, Weller S, Fayard E (2008) Human recombinant erythropoietin and the incidence of retinopathy of prematurity: a multiple regression model. J AAPOS 12:233–238CrossRefPubMed Suk KK, Dunbar JA, Liu A, Daher NS, Leng CK, Leng JK, Lim P, Weller S, Fayard E (2008) Human recombinant erythropoietin and the incidence of retinopathy of prematurity: a multiple regression model. J AAPOS 12:233–238CrossRefPubMed
33.
go back to reference Arjamaa O, Nikinmaa M (2006) Oxygen-dependent diseases in the retina: role of hypoxia-inducible factors. Exp Eye Res 83:473–483CrossRefPubMed Arjamaa O, Nikinmaa M (2006) Oxygen-dependent diseases in the retina: role of hypoxia-inducible factors. Exp Eye Res 83:473–483CrossRefPubMed
34.
go back to reference Sears JE, Hoppe G, Ebrahem Q, Anand-Apte B (2008) Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy. Proc Natl Acad Sci U S A 105:19898–19903CrossRefPubMed Sears JE, Hoppe G, Ebrahem Q, Anand-Apte B (2008) Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy. Proc Natl Acad Sci U S A 105:19898–19903CrossRefPubMed
35.
go back to reference Morita M, Ohneda O, Yamashita T, Takahashi S, Suzuki N, Nakajima O, Kawauchi S, Ema M, Shibahara S, Udono T, Tomita K, Tamai M, Sogawa K, Yamamoto M, Fujii-Kuriyama Y (2003) HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J 22:1134–1146CrossRefPubMed Morita M, Ohneda O, Yamashita T, Takahashi S, Suzuki N, Nakajima O, Kawauchi S, Ema M, Shibahara S, Udono T, Tomita K, Tamai M, Sogawa K, Yamamoto M, Fujii-Kuriyama Y (2003) HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J 22:1134–1146CrossRefPubMed
36.
go back to reference Dioum EM, Clarke SL, Ding K, Repa JJ, Garcia JA (2008) HIF-2alpha-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery. Invest Ophthalmol Vis Sci 49:2714–2720CrossRefPubMed Dioum EM, Clarke SL, Ding K, Repa JJ, Garcia JA (2008) HIF-2alpha-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery. Invest Ophthalmol Vis Sci 49:2714–2720CrossRefPubMed
37.
go back to reference Stone WL, Farnsworth CC, Dratz EA (1979) A reinvestigation of the fatty acid content of bovine, rat and frog retinal rod outer segments. Exp Eye Res 28:387–397CrossRefPubMed Stone WL, Farnsworth CC, Dratz EA (1979) A reinvestigation of the fatty acid content of bovine, rat and frog retinal rod outer segments. Exp Eye Res 28:387–397CrossRefPubMed
38.
go back to reference Fliesler SJ, Anderson RE (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22:79–131CrossRefPubMed Fliesler SJ, Anderson RE (1983) Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22:79–131CrossRefPubMed
39.
go back to reference SanGiovanni JP, Chew EY (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res 24:87–138CrossRefPubMed SanGiovanni JP, Chew EY (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res 24:87–138CrossRefPubMed
40.
go back to reference Clandinin MT, Chappell JE, Leong S, Heim T, Swyer PR, Chance GW (1980) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum Dev 4:121–129CrossRefPubMed Clandinin MT, Chappell JE, Leong S, Heim T, Swyer PR, Chance GW (1980) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum Dev 4:121–129CrossRefPubMed
41.
go back to reference Martinez M (1992) Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr 120:S129–S138CrossRefPubMed Martinez M (1992) Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr 120:S129–S138CrossRefPubMed
42.
go back to reference Krauss-Etschmann S, Shadid R, Campoy C, Hoster E, Demmelmair H, Jimenez M, Gil A, Rivero M, Veszpremi B, Decsi T, Koletzko BV (2007) Effects of fish-oil and folate supplementation of pregnant women on maternal and fetal plasma concentrations of docosahexaenoic acid and eicosapentaenoic acid: a European randomized multicenter trial. Am J Clin Nutr 85:1392–1400PubMed Krauss-Etschmann S, Shadid R, Campoy C, Hoster E, Demmelmair H, Jimenez M, Gil A, Rivero M, Veszpremi B, Decsi T, Koletzko BV (2007) Effects of fish-oil and folate supplementation of pregnant women on maternal and fetal plasma concentrations of docosahexaenoic acid and eicosapentaenoic acid: a European randomized multicenter trial. Am J Clin Nutr 85:1392–1400PubMed
43.
go back to reference Uauy R, Peirano P, Hoffman D, Mena P, Birch D, Birch E (1996) Role of essential fatty acids in the function of the developing nervous system. Lipids 31:S167–S176CrossRefPubMed Uauy R, Peirano P, Hoffman D, Mena P, Birch D, Birch E (1996) Role of essential fatty acids in the function of the developing nervous system. Lipids 31:S167–S176CrossRefPubMed
44.
go back to reference Uauy R, Hoffman DR, Peirano P, Birch DG, Birch EE (2001) Essential fatty acids in visual and brain development. Lipids 36:885–895CrossRefPubMed Uauy R, Hoffman DR, Peirano P, Birch DG, Birch EE (2001) Essential fatty acids in visual and brain development. Lipids 36:885–895CrossRefPubMed
45.
go back to reference Connor KM, SanGiovanni JP, Lofqvist C, Aderman CM, Chen J, Higuchi A, Hong S, Pravda EA, Majchrzak S, Carper D, Hellstrom A, Kang JX, Chew EY, Salem N Jr, Serhan CN, Smith LE (2007) Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 13:868–873CrossRefPubMed Connor KM, SanGiovanni JP, Lofqvist C, Aderman CM, Chen J, Higuchi A, Hong S, Pravda EA, Majchrzak S, Carper D, Hellstrom A, Kang JX, Chew EY, Salem N Jr, Serhan CN, Smith LE (2007) Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 13:868–873CrossRefPubMed
46.
go back to reference Penn JS, Tolman BL, Bullard LE (1997) Effect of a water-soluble vitamin E analog, trolox C, on retinal vascular development in an animal model of retinopathy of prematurity. Free Radic Biol Med 22:977–984CrossRefPubMed Penn JS, Tolman BL, Bullard LE (1997) Effect of a water-soluble vitamin E analog, trolox C, on retinal vascular development in an animal model of retinopathy of prematurity. Free Radic Biol Med 22:977–984CrossRefPubMed
47.
go back to reference Niesman MR, Johnson KA, Penn JS (1997) Therapeutic effect of liposomal superoxide dismutase in an animal model of retinopathy of prematurity. Neurochem Res 22:597–605CrossRefPubMed Niesman MR, Johnson KA, Penn JS (1997) Therapeutic effect of liposomal superoxide dismutase in an animal model of retinopathy of prematurity. Neurochem Res 22:597–605CrossRefPubMed
48.
go back to reference Spierer A, Rabinowitz R, Pri-Chen S, Rosner M (2005) An increase in superoxide dismutase ameliorates oxygen-induced retinopathy in transgenic mice. Eye 19:86–91CrossRefPubMed Spierer A, Rabinowitz R, Pri-Chen S, Rosner M (2005) An increase in superoxide dismutase ameliorates oxygen-induced retinopathy in transgenic mice. Eye 19:86–91CrossRefPubMed
49.
go back to reference Ando A, Yang A, Mori K, Yamada H, Yamada E, Takahashi K, Saikia J, Kim M, Melia M, Fishman M, Huang P, Campochiaro PA (2002) Nitric oxide is proangiogenic in the retina and choroid. J Cell Physiol 191:116–124CrossRefPubMed Ando A, Yang A, Mori K, Yamada H, Yamada E, Takahashi K, Saikia J, Kim M, Melia M, Fishman M, Huang P, Campochiaro PA (2002) Nitric oxide is proangiogenic in the retina and choroid. J Cell Physiol 191:116–124CrossRefPubMed
50.
go back to reference Beauchamp MH, Sennlaub F, Speranza G, Gobeil F Jr, Checchin D, Kermorvant-Duchemin E, Abran D, Hardy P, Lachapelle P, Varma DR, Chemtob S (2004) Redox-dependent effects of nitric oxide on microvascular integrity in oxygen-induced retinopathy. Free Radic Biol Med 37:1885–1894CrossRefPubMed Beauchamp MH, Sennlaub F, Speranza G, Gobeil F Jr, Checchin D, Kermorvant-Duchemin E, Abran D, Hardy P, Lachapelle P, Varma DR, Chemtob S (2004) Redox-dependent effects of nitric oxide on microvascular integrity in oxygen-induced retinopathy. Free Radic Biol Med 37:1885–1894CrossRefPubMed
51.
go back to reference Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87:1620–1624CrossRefPubMed Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87:1620–1624CrossRefPubMed
52.
go back to reference Kirsch M, Korth HG, Sustmann R, de Groot H (2002) The pathobiochemistry of nitrogen dioxide. Biol Chem 383:389–399CrossRefPubMed Kirsch M, Korth HG, Sustmann R, de Groot H (2002) The pathobiochemistry of nitrogen dioxide. Biol Chem 383:389–399CrossRefPubMed
53.
go back to reference Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB (2003) Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol 285:C546–C554PubMed Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB (2003) Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol 285:C546–C554PubMed
54.
go back to reference Holmes JM, Duffner LA, Kappil JC (1994) The effect of raised inspired carbon dioxide on developing rat retinal vasculature exposed to elevated oxygen. Curr Eye Res 13:779–782CrossRefPubMed Holmes JM, Duffner LA, Kappil JC (1994) The effect of raised inspired carbon dioxide on developing rat retinal vasculature exposed to elevated oxygen. Curr Eye Res 13:779–782CrossRefPubMed
55.
go back to reference Holmes JM, Zhang S, Leske DA, Lanier WL (1997) The effect of carbon dioxide on oxygen-induced retinopathy in the neonatal rat. Curr Eye Res 16:725–732CrossRefPubMed Holmes JM, Zhang S, Leske DA, Lanier WL (1997) The effect of carbon dioxide on oxygen-induced retinopathy in the neonatal rat. Curr Eye Res 16:725–732CrossRefPubMed
56.
go back to reference Checchin D, Hou X, Hardy P, Abran D, Najarian T, Beauchamp MH, Bernier SG, Gobeil F Jr, Quiniou C, Varma DR, Chemtob S (2002) PGE2-mediated eNOS induction in prolonged hypercapnia. Invest Ophthalmol Vis Sci 43:1558–1566PubMed Checchin D, Hou X, Hardy P, Abran D, Najarian T, Beauchamp MH, Bernier SG, Gobeil F Jr, Quiniou C, Varma DR, Chemtob S (2002) PGE2-mediated eNOS induction in prolonged hypercapnia. Invest Ophthalmol Vis Sci 43:1558–1566PubMed
57.
go back to reference Checchin D, Sennlaub F, Sirinyan M, Brault S, Zhu T, Kermorvant-Duchemin E, Hardy P, Balazy M, Chemtob S (2006) Hypercapnia prevents neovascularization via nitrative stress. Free Radic Biol Med 40:543–553CrossRefPubMed Checchin D, Sennlaub F, Sirinyan M, Brault S, Zhu T, Kermorvant-Duchemin E, Hardy P, Balazy M, Chemtob S (2006) Hypercapnia prevents neovascularization via nitrative stress. Free Radic Biol Med 40:543–553CrossRefPubMed
58.
go back to reference Brooks SE, Gu X, Samuel S, Marcus DM, Bartoli M, Huang PL, Caldwell RB (2001) Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci 42:222–228PubMed Brooks SE, Gu X, Samuel S, Marcus DM, Bartoli M, Huang PL, Caldwell RB (2001) Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci 42:222–228PubMed
59.
60.
go back to reference Jiang H, Kruger N, Lahiri DR, Wang D, Vatele JM, Balazy M (1999) Nitrogen dioxide induces cis–trans-isomerization of arachidonic acid within cellular phospholipids. Detection of trans-arachidonic acids in vivo. J Biol Chem 274:16235–16241CrossRefPubMed Jiang H, Kruger N, Lahiri DR, Wang D, Vatele JM, Balazy M (1999) Nitrogen dioxide induces cis–trans-isomerization of arachidonic acid within cellular phospholipids. Detection of trans-arachidonic acids in vivo. J Biol Chem 274:16235–16241CrossRefPubMed
61.
go back to reference Zghibeh CM, Raj Gopal V, Poff CD, Falck JR, Balazy M (2004) Determination of trans-arachidonic acid isomers in human blood plasma. Anal Biochem 332:137–144CrossRefPubMed Zghibeh CM, Raj Gopal V, Poff CD, Falck JR, Balazy M (2004) Determination of trans-arachidonic acid isomers in human blood plasma. Anal Biochem 332:137–144CrossRefPubMed
62.
go back to reference Balazy M (2000) Trans-arachidonic acids: new mediators of inflammation. J Physiol Pharmacol 51:597–607PubMed Balazy M (2000) Trans-arachidonic acids: new mediators of inflammation. J Physiol Pharmacol 51:597–607PubMed
63.
64.
go back to reference Vincent JL, Zhang H, Szabo C, Preiser JC (2000) Effects of nitric oxide in septic shock. Am J Respir Crit Care Med 161:1781–1785PubMed Vincent JL, Zhang H, Szabo C, Preiser JC (2000) Effects of nitric oxide in septic shock. Am J Respir Crit Care Med 161:1781–1785PubMed
65.
go back to reference Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, Brault S, Andelfinger G, Kooli A, Germain S, Ong H, d’Orleans-Juste P, Gobeil F Jr, Zhu T, Boisvert C, Hardy P, Jain K, Falck JR, Balazy M, Chemtob S (2005) Trans-arachidonic acids generated during nitrative stress induce a thrombospondin-1-dependent microvascular degeneration. Nat Med 11:1339–1345CrossRefPubMed Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, Brault S, Andelfinger G, Kooli A, Germain S, Ong H, d’Orleans-Juste P, Gobeil F Jr, Zhu T, Boisvert C, Hardy P, Jain K, Falck JR, Balazy M, Chemtob S (2005) Trans-arachidonic acids generated during nitrative stress induce a thrombospondin-1-dependent microvascular degeneration. Nat Med 11:1339–1345CrossRefPubMed
66.
go back to reference Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138:707–717CrossRefPubMed Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138:707–717CrossRefPubMed
67.
go back to reference Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41–48CrossRefPubMed Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41–48CrossRefPubMed
68.
go back to reference Wang S, Wu Z, Sorenson CM, Lawler J, Sheibani N (2003) Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration. Dev Dyn 228:630–642CrossRefPubMed Wang S, Wu Z, Sorenson CM, Lawler J, Sheibani N (2003) Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration. Dev Dyn 228:630–642CrossRefPubMed
69.
go back to reference Cai W, Rook SL, Jiang ZY, Takahara N, Aiello LP (2000) Mechanisms of hepatocyte growth factor-induced retinal endothelial cell migration and growth. Invest Ophthalmol Vis Sci 41:1885–1893PubMed Cai W, Rook SL, Jiang ZY, Takahara N, Aiello LP (2000) Mechanisms of hepatocyte growth factor-induced retinal endothelial cell migration and growth. Invest Ophthalmol Vis Sci 41:1885–1893PubMed
70.
go back to reference D’Amore PA (1994) Mechanisms of retinal and choroidal neovascularization. Invest Ophthalmol Vis Sci 35:3974–3979PubMed D’Amore PA (1994) Mechanisms of retinal and choroidal neovascularization. Invest Ophthalmol Vis Sci 35:3974–3979PubMed
71.
go back to reference Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes HP, Shani M, Fassler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307–4316CrossRefPubMed Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes HP, Shani M, Fassler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21:4307–4316CrossRefPubMed
72.
go back to reference Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438:960–966CrossRefPubMed Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438:960–966CrossRefPubMed
73.
go back to reference Lee MS, Moon EJ, Lee SW, Kim MS, Kim KW, Kim YJ (2001) Angiogenic activity of pyruvic acid in in vivo and in vitro angiogenesis models. Cancer Res 61:3290–3293PubMed Lee MS, Moon EJ, Lee SW, Kim MS, Kim KW, Kim YJ (2001) Angiogenic activity of pyruvic acid in in vivo and in vitro angiogenesis models. Cancer Res 61:3290–3293PubMed
74.
go back to reference Murray B, Wilson DJ (2001) A study of metabolites as intermediate effectors in angiogenesis. Angiogenesis 4:71–77CrossRefPubMed Murray B, Wilson DJ (2001) A study of metabolites as intermediate effectors in angiogenesis. Angiogenesis 4:71–77CrossRefPubMed
75.
go back to reference Neuman RE, Mc CT (1958) Growth-promoting properties of pyruvate oxal-acetate, and alpha-ketoglutarate for isolated Walker carcinosarcoma 256 cells. Proc Soc Exp Biol Med 98:303–306PubMed Neuman RE, Mc CT (1958) Growth-promoting properties of pyruvate oxal-acetate, and alpha-ketoglutarate for isolated Walker carcinosarcoma 256 cells. Proc Soc Exp Biol Med 98:303–306PubMed
76.
go back to reference He W, Miao FJ, Lin DC, Schwandner RT, Wang Z, Gao J, Chen JL, Tian H, Ling L (2004) Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature 429:188–193CrossRefPubMed He W, Miao FJ, Lin DC, Schwandner RT, Wang Z, Gao J, Chen JL, Tian H, Ling L (2004) Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature 429:188–193CrossRefPubMed
77.
go back to reference Sapieha P, Sirinyan M, Hamel D, Zaniolo K, Joyal JS, Cho JH, Honore JC, Kermorvant-Duchemin E, Varma DR, Tremblay S, Leduc M, Rihakova L, Hardy P, Klein WH, Mu X, Mamer O, Lachapelle P, Di Polo A, Beausejour C, Andelfinger G, Mitchell G, Sennlaub F, Chemtob S (2008) The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med 14:1067–1076CrossRefPubMed Sapieha P, Sirinyan M, Hamel D, Zaniolo K, Joyal JS, Cho JH, Honore JC, Kermorvant-Duchemin E, Varma DR, Tremblay S, Leduc M, Rihakova L, Hardy P, Klein WH, Mu X, Mamer O, Lachapelle P, Di Polo A, Beausejour C, Andelfinger G, Mitchell G, Sennlaub F, Chemtob S (2008) The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med 14:1067–1076CrossRefPubMed
Metadata
Title
Understanding ischemic retinopathies: emerging concepts from oxygen-induced retinopathy
Authors
Elsa Kermorvant-Duchemin
Przemyslaw Sapieha
Mirna Sirinyan
Martin Beauchamp
Daniella Checchin
Pierre Hardy
Florian Sennlaub
Pierre Lachapelle
Sylvain Chemtob
Publication date
01-02-2010
Publisher
Springer-Verlag
Published in
Documenta Ophthalmologica / Issue 1/2010
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-009-9201-x

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